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Reptile-Associated Salmonellosis -- Selected States, 1994-1995

During 1994-1995, health departments in 13 states reported to CDC persons infected with unusual Salmonella serotypes in which the patients had direct or indirect contact with reptiles (i.e., lizards, snakes, or turtles). In many of those cases, the same serotype of Salmonella was isolated from patients and from reptiles with which they had had contact or a common contact. For some cases, infection resulted in invasive illness, such as sepsis and meningitis. This report summarizes clinical and epidemiologic information for six of these cases.

Connecticut. During January 1995, a 40-year-old man was hospitalized because of an acute illness characterized by constipation, lower back pain, chills, and fever. He reported having taken ranitidine and an antacid for symptoms of heartburn before onset of mild diarrhea 3 days before hospitalization. A blood culture yielded Salmonella serotype Wassenaar. A magnetic resonance image scan of the right sacrum suggested osteomyelitis. Ciprofloxacin therapy was initiated for presumed Salmonella osteomyelitis, and he was discharged after 14 days. All household contacts were asymptomatic. The family had purchased two iguanas (Iguana iguana) in October 1994; although the patient denied directly handling the iguanas, he reported having recently cleaned their aquarium. Stool samples obtained from both iguanas yielded Salmonella Wassenaar.

New Jersey. During September 1994, a 5-month-old girl was hospitalized because of an acute illness including vomiting, lethargy, and fever; on admission, she had a bulging fontanelle and stiff neck. Blood cultures and cerebrospinal fluid yielded Salmonella serotype Rubislaw. She was treated with intravenous ceftazidime for Salmonella sepsis and meningitis and discharged from the hospital after 10 days. Other members of the family were asymptomatic. The infant routinely was fed infant formula. Although the family did not own a reptile, the infant frequently stayed at a babysitter's house where an iguana was kept. Culture of a stool sample from the iguana yielded Salmonella Rubislaw. The infant was reported to have not touched the iguana; however, the iguana frequently was handled by the babysitter and other members of the babysitter's family. All members of the babysitter's family were asymptomatic, but stool cultures from two members, including a child who had frequently played with and fed the infant, yielded Salmonella Rubislaw.

New York. In December 1994, a 45-year-old man infected with human immunodeficiency virus was hospitalized because of weakness, nausea, vomiting, and diarrhea. His CD4+ T-lymphocyte count was less than 50 cells/uL. Cultures from blood and sputum samples yielded Salmonella serotype IIIa 41:z subscript 4 z subscript 23:- (S. subspecies Arizonae). He owned corn snakes and, until shortly before onset of illness, had worked at a pet store where he handled reptiles frequently. Salmonella sepsis was diagnosed, and he was treated with oral ciprofloxacin.

North Carolina. During December 1994, a 2-day-old boy born 8 weeks prematurely developed respiratory difficulties, had pneumothorax diagnosed, and was transferred to a referral hospital. Blood obtained at birth for culture had been negative, but a culture of blood obtained 9 days later because of an elevated white blood cell count yielded Salmonella serotype Kintambo. He was treated with intravenous ampicillin for Salmonella sepsis and was discharged from the hospital after 30 days. Eleven days after the positive culture was collected, Salmonella Kintambo was cultured from a blood sample obtained from a 12-day-old acutely ill boy who was born at 28 weeks' gestation and had shared a room at the referral hospital with the first infant. The second infant was treated with intravenous cefotaxime for Salmonella sepsis and was discharged after 44 days. Both infants had been in the hospital continuously from birth until onset of illness. The mother of the first infant reported having had a diarrheal illness 4 days before the birth of the infant; she frequently handled a savanna monitor lizard (Varanus exanthemapicus) that the family had purchased in September 1994 and kept in a cage in the kitchen. Culture of a stool sample from the lizard yielded Salmonella Kintambo. The second family did not own a reptile.

Ohio. During January 1994, a 6-week-old boy was hospitalized because of diarrhea, stiff neck, and fever; culture of samples of blood and cerebrospinal fluid yielded Salmonella serotype Stanley. The infant was treated with intravenous cefotaxime for Salmonella sepsis and meningitis and discharged from the hospital after 56 days. He had been fed only formula and had not attended a child-care facility; household contacts were asymptomatic. The family had purchased a 4-inch water turtle in April 1993. A culture of stool from the turtle yielded Salmonella Stanley. Although the infant had not had contact with the turtle, other family members had had direct contact, and the turtle's food and water bowls were washed in the kitchen sink.

Pennsylvania. During October 1994, a 21-day-old girl was hospitalized because of an illness including vomiting, bloody diarrhea, and fever. She received empirical treatment with intravenous ampicillin. A culture of stool yielded Salmonella serotype Poona; she was discharged from the hospital after 11 days. Other members of the family were asymptomatic. The infant had been fed infant formula and had not attended a child-care center. The family owned an iguana, and culture of a stool sample from the iguana yielded Salmonella Poona. Although the infant did not have contact with the iguana, the iguana was handled frequently by her mother and other members of the family.

Additional investigations. In addition to the six states in this report, seven other states (California, Colorado, Florida, Illinois, Minnesota, Oregon, and Utah) have reported recent isolation of the same Salmonella serotype from samples obtained from patients and reptiles with which they had been in contact or associated. Several of these states issued press releases about the risk for acquiring salmonellosis from reptiles. In addition, some states have issued health alerts to pet stores to warn owners and prospective owners about the risks for salmonellosis associated with contact with reptiles and to provide instructions about proper handling of reptiles; store owners have been asked to post the alert and provide copies to all persons purchasing a reptile. Reported by: JW Weinstein, MD, EG Seltzer, MD, Yale Univ School of Medicine, New Haven; RS Nelson, DVM, JL Hadler, MD, State Epidemiologist, Connecticut Dept of Public Health and Addiction Svcs. SM Paul, MD, FE Sorhage, VMD, Div of Epidemiology, Environmental and Occupational Health Svcs; K Pilot, S Matluck, Public Health and Environmental Laboratories; K Spitalny, MD, State Epidemiologist, New Jersey State Dept of Health. M Gupta, MD, J Misage, G Balzano, T Root, G Birkhead, MD, DL Morse, MD, State Epidemiologist, New York State Dept of Health. A Kopelman, MD, S Engelke, MD, L Jones, Pitt County Memorial Hospital, Greenville; L Latour, PhD, P Perry, Wilson County Health Dept, Wilson; B Jenkins, State Laboratory of Public Health, J-M Maillard, MD, JN MacCormack, MD, State Epidemiologist, North Carolina Dept of Environment, Health, and Natural Resources. C Richards, P Fruth, Defiance County Health Dept, Defiance; S Hufford, MD, B Dick, MPH, Toledo Hospital; M Bundesen, Bur of Public Health Laboratories, EP Salehi, MPH, Infectious Disease Epidemiology Unit, TJ Halpin, MD, State Epidemiologist, Ohio Dept of Health. P Lurie, MD, M Deasy, K Mihelcic, JT Rankin, Jr, DVM, State Epidemiologist, Pennsylvania Dept of Health. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; Div of Field Epidemiology, Epidemiology Program Office, CDC.

Editorial Note

Editorial Note: For most of the cases described in this report, the identification of rare Salmonella serotypes in persons who had no other apparent exposures was linked to direct or indirect contact with a pet reptile from which the same serotype was isolated. In addition, these cases are consistent with previous reports indicating that direct contact with a reptile is not necessary for transmission of Salmonella (1,2). This report also illustrates the severe complications of Salmonella infection that can occur in young children, immunocompromised persons, and infants during the peripartum period.

Reptiles are popular as pets in the United States: an estimated 7.3 million pet reptiles are owned by approximately 3% of households (G. Mitchell, Pet Industry Joint Advisory Council, personal communication, 1995). Because the most popular reptiles species will not breed if closely confined, most reptiles are captured in the wild and imported. The number of reptiles imported into the United States has increased dramatically since 1986 and primarily reflects importation of iguanas (27,806 in 1986 to 798,405 in 1993) (M. Albert, Fish and Wildlife Service, U.S. Department of the Interior, personal communication, June, 1994).

A high proportion of reptiles are asymptomatic carriers of Salmonella. Fecal carriage rates can be more than 90% (3); attempts to eliminate Salmonella carriage in reptiles with antibiotics have been unsuccessful and have led to increased antibiotic resistance (1,4). A wide variety of Salmonella serotypes has been isolated from reptiles, including many that rarely are isolated from other animals (reptile-associated serotypes). Reptiles can become infected through transovarial transmission or direct contact with other infected reptiles or contaminated reptile feces. High rates of fecal carriage of Salmonella can be related to the eating of feces by hatchlings -- a typical behavior for iguanas and other lizards -- which can establish normal intestinal flora for hindgut fermentation (5).

During the early 1970s, small pet turtles were an important source of Salmonella infection in the United States; an estimated 4% of families owned turtles, and 14% of salmonellosis cases were attributed to exposure to turtles (6). In 1975, the Food and Drug Administration prohibited the distribution and sale of turtles with a carapace less than 4 inches; many states prohibited the sale of such turtles. These measures resulted in the prevention of an estimated 100,000 cases of salmonellosis annually (6). However, since 1986, the popularity of iguanas and other reptiles that can transmit infection to humans has been paralleled by an increased incidence of Salmonella infections caused by reptile-associated serotypes (7).

Because young children are at increased risk for reptile-associated salmonellosis and severe complications (e.g., septicemia and meningitis) (7-9), reducing exposure of infants or children aged less than 5 years to reptiles is particularly important. The risks for transmission of Salmonella from reptiles to humans can be reduced by avoiding direct and indirect contact with reptiles (see box). (BOX) Recommendations for Preventing Transmission of Salmonella From Reptiles to Humans

  • Persons at increased risk for infection or serious complications of salmonellosis (e.g., pregnant women, children aged less than 5 years, and immunocompromised persons such as persons with AIDS) should avoid contact with reptiles.

  • Reptiles should not be kept in child-care centers and may not be appropriate pets in households in which persons at increased risk for infection reside.

  • Veterinarians and pet store owners should provide information to potential purchasers and owners of reptiles about the increased risk of acquiring salmonellosis from reptiles.

  • Veterinarians and operators of pet stores should advise reptile owners always to wash their hands after handling reptiles and reptile cages.

  • To prevent contamination of food-preparation areas (e.g., kitchens) and other selected sites, reptiles should be kept out of these areas in particular, kitchen sinks should not be used to bathe reptiles or to wash reptile dishes, cages, or aquariums.


References

  1. CDC. Iguana-associated salmonellosis -- Indiana, 1990. MMWR 1992;41:38-9.

  2. CDC. Lizard-associated salmonellosis -- Utah. MMWR 1992;41:610-1.

  3. Chiodini RJ, Sundberg JP. Salmonellosis in reptiles: a review. Am J Epidemiol 1981;113:494-9.

  4. Shane SM, Gilbert R, Harrington KS. Salmonella colonization in commercial pet turtles (Pseudemys scripta elegans). Epidemiol Infect 1990;105:307-16.

  5. Troyer K. Transfer of fermentative microbes between generations in herbivorous lizard. Science 1982;216:540-2.

  6. Cohen ML, Potter M, Pollard R, Feldman RA. Turtle-associated salmonellosis in the United States: effect of public health action, 1970 to 1976. JAMA 1980;243:1247-9.

  7. Cieslak PR, Angulo FJ, Dueger EL, Maloney EK, Swerdlow DL. Leapin' lizards: a jump in the incidence of reptile-associated salmonellosis {Abstract}. In: Program and abstracts of the 34th Interscience Conference on Antimicrobial Agents and Chemotherapy. Washington, DC: American Society for Microbiology, 1994.

  8. Ackman D, Drabkin P, Birkhead B, Cieslak P. Reptile-associated salmonellosis: a case-control study {Abstract}. In: Program and abstracts of the 34th Interscience Conference on Antimicrobial Agents and Chemotherapy. Washington, DC: American Society for Microbiology, 1994.

  9. Dalton C, Hoffman R, Pape J. Iguana-associated salmonellosis in children. Pediatr Infect Dis J 1995;14:319-20.




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